Paweł Koteja

GENETIC CORRELATIONS BETWEEN BASAL AND MAXIMUM METABOLIC RATES IN A WILD RODENT: CONSEQUENCES FOR EVOLUTION OF ENDOTHERMY

Abstract According to the aerobic capacity model, endothermy in birds and mammals evolved as a correlated response to selection for an ability of sustained locomotor activity, rather than in a response to direct selection for thermoregulatory capabilities. A key assumption of the model is that aerobic capacity is functionally linked to basal metabolic rate (BMR). The assumption has been tested in several studies at the level of phenotypic variation among individuals or species, but none has provided a clear answer whether the traits are genetically correlated. Here we present results of a genetic analysis based on measurements of the basal and the maximum swim‐ and cold‐induced oxygen consumption in about 1000 bank voles from six generations of a laboratory colony, reared from animals captured in the field. Narrow sense heritability (h2) was about 0.5 for body mass, about 0.4 for mass‐independent basal and maximum metabolic rates, and about 0.3 for factorial aerobic scopes. Dominance genetic and common environmental (5 maternal) effects were not significant. Additive genetic correlation between BMR and the swim‐induced aerobic capacity was high and positive, whereas correlation resulting from specific‐environmental effects was negative. However, BMR was not genetically correlated with the cold‐induced aerobic capacity. The results are consistent with the aerobic capacity model of the evolution of endothermy in birds and mammals.

Energy assimilation, parental care and the evolution of endothermy

The question of the selection forces which initiated the evolution of endothermy in birds and mammals is one of the most intriguing in the evolutionary physiology of vertebrates. Many students regard the aerobic capacity model as the most plausible hypothesis. This paper presents an alternative model, in which the evolution of endothermy in birds and mammals was driven by two factors: (i) a selection for intense post–hatching parental care, particularly feeding offspring, and (ii) the high cost of maintaining the increased capacity of the visceral organs necessary to support high rates of total daily energy expenditures.

Energy Cost of Wheel Running in House Mice: Implications for Coadaptation of Locomotion and Energy Budgets

Laboratory house mice (Mus domesticus) that had experienced 10 generations of artificial selection for high levels of voluntary wheel running ran about 70% more total revolutions per day than did mice from random‐bred control lines. The difference resulted primarily from increased average velocities rather than from increased time spent running. Within all eight lines (four selected, four control), females ran more than males. Average daily running distances ranged from 4.4 km in control males to 11.6 km in selected females. Whole‐animal food consumption was statistically indistinguishable in the selected and control lines. However, mice from selected lines averaged approximately 10% smaller in body mass, and mass‐adjusted food consumption was 4% higher in selected lines than in controls. The incremental cost of locomotion (grams food/revolution), computed as the partial regression slope of food consumption on revolutions run per day, did not differ between selected and control mice. On a 24‐h basis, the total incremental cost of running (covering a distance) amounted to only 4.4% of food consumption in the control lines and 7.5% in the selected ones. However, the daily incremental cost of time active is higher (15.4% and 13.1% of total food consumption in selected and control lines, respectively). If wheel running in the selected lines continues to increase mainly by increases in velocity, then constraints related to energy acquisition are unlikely to be an important factor limiting further selective gain. More generally, our results suggest that, in small mammals, a substantial evolutionary increase in daily movement distances can be achieved by increasing running speed, without remarkable increases in total energy expenditure.

Limits to the Energy Budget in a Rodent, Peromyscus maniculatus: Does Gut Capacity Set the Limit?

Nonreproducing Peromyscus maniculatus acclimated to 23° C and a standard mouse food can maintain a positive energy balance at-10° C. Their maximum cold-induced rate of energy assimilation is about 90 kJ/d, which is twice the energy expenditure at 23°C and five times their basal metabolic rate. Cold-acclimated individuals have an enlarged alimentary tract and at-18° C achieve a maximum cold-induced rate of energy assimilation of 113 kJ/d. The pattern of energy budget limitations depends on sex: males adopt a more frugal strategy of energy use. In females acclimated to afiber-diluted diet, the size of the alimentary tract and the maximum cold-induced rate of energy assimilation are increased. In males the effect is opposite. There is a strong correlation between an individuals maximum cold-induced rate of energy assimilation and the size of the alimentary tract, liver, and kidney; the correlation is strongest for the mass of the small intestine. These results are consistent with the hypothesis that energy budgets are limited by the process of food digestion and/or absorption in the small intestine. The intraspecific correlation between basal metabolic rate and maximum rate of energy assimilation and between basal metabolic rate and the size of the alimentary tract was not high.

Individual variation and repeatability of basal metabolism in the bank vole, Clethrionomys glareolus

Basal metabolic rate (BMR) is a fundamental energetic trait and has been measured in hundreds of birds and mammals. Nevertheless, little is known about the consistency of the population–average BMR or its repeatability at the level of individual variation. Here, we report that average mass–independent BMR did not differ between two generations of bank voles or between two trials separated by one month. Individual differences in BMR were highly repeatable across the one month interval: the coefficient of intraclass correlation was 0.70 for absolute log–transformed values and 0.56 for mass–independent values. Thus, BMR can be a meaningful measure of an individual physiological characteristic and can be used to test hypotheses concerning relationships between BMR and other traits. On the other hand, mass–independent BMR did not differ significantly across families, and the coefficient of intraclass correlation for full sibs did not differ from zero, which suggests that heritability of BMR in voles is not high.

On the relation between basal and maximum metabolic rate in mammals

Basal and maximum metabolic rates, measured by oxygen consumption, for 18 species of wild mammals have been obtained from a search of literature records. The mass exponent of the allometric regression equation for maximum metabolic rate is significantly higher than that for BMR (0.841 and 0.745, respectively; P less than 0.05) in the group of animals examined. No significant correlation between mass-independent basal and maximum metabolic rates has been found. These results do not support the aerobic capacity model of the origin of endothermy.

The Evolution of Concepts on the Evolution of Endothermy in Birds and Mammals

Warm‐blooded animals, mammals and birds, are unique not because they are endothermic in the strict sense of the term but because they use an extravagant economy: they have high energy budgets and spend a large part of their energy resources on basic maintenance. Although several advantages of endothermy are easy to indicate, mechanisms behind evolution of such a wasteful life strategy remain unclear and have been subject to intensive debate. For two decades, the aerobic capacity model has been widely recognized as a promising hypothesis and has catalyzed a new direction in ecological and evolutionary physiology—the study of correlated evolution of behavioral and morphophysiological traits. Recently, two alternative models have been proposed, both of which see evolution of high metabolic rates in birds and mammals as an element in evolution of intensive parental care. Unlike previous models, which treated individuals as static objects of fixed properties, the parental care models explicitly incorporate life histories into a evolutionary‐physiology research program. The aim of this article was to outline the process of evolution of major concepts in the field, which reflects development of the paradigm of modern evolutionary physiology.

Is reproduction costly? No increase of oxidative damage in breeding bank voles

SUMMARY According to life-history theory, investment in reproduction is associated with costs, which should appear as decreased survival to the next reproduction or lower future reproductive success. It has been suggested that oxidative stress may be the proximate mechanism of these trade-offs. Despite numerous studies of the defense against reactive oxygen species (ROS) during reproduction, very little is known about the damage caused by ROS to the tissues of wild breeding animals. We measured oxidative damage to lipids and proteins in breeding bank vole (Myodes glareolus) females after rearing one and two litters, and in non-breeding females. We used bank voles from lines selected for high maximum aerobic metabolic rates (which also had high resting metabolic rates and food intake) and non-selected control lines. The oxidative damage was determined in heart, kidneys and skeletal muscles by measuring the concentration of thiobarbituric acid-reactive substances, as markers of lipid peroxidation, and carbonyl groups in proteins, as markers of protein oxidation. Surprisingly, we found that the oxidative damage to lipids in kidneys and muscles was actually lower in breeding than in non-breeding voles, and it did not differ between animals from the selected and control lines. Thus, contrary to our predictions, females that bred suffered lower levels of oxidative stress than those that did not reproduce. Elevated production of antioxidant enzymes and the protective role of sex hormones may explain the results. The results of the present study do not support the hypothesis that oxidative damage to tissues is the proximate mechanism of reproduction costs.

Limits to the Energy Budget in a Rodent, Peromyscus maniculatus: The Central Limitation Hypothesis

The maximum rate of energy assimilation in lactating Peromyscus maniculatus (100 kJ/d, body mass = 25 g) was lower than in cold-exposed females (115 kJ/d, body mass = 20 g). This pattern differs from that found in a few species of voles and mice, in which lactating females achieve higher rates of assimilation than cold-exposed animals. The results do not support the hypothesis that energy budgets of animals are limited centrally by the rate of energy assimilation from food, irrespective of which metabolic function constitutes the main energy expenditure. The discussion about physiological limits to energy budgets must involve information about the life strategies of the animals.

Using new tools to solve an old problem: the evolution of endothermy in vertebrates

During the past 30 years, the evolution of endothermy has been a topic of keen interest to palaeontologists and evolutionary physiologists. While palaeontologists have found abundant Permian and Triassic fossils, suggesting important clues regarding the timing of origin of endothermy, physiologists have proposed several plausible hypotheses of how the metabolic elevation leading to endothermy could have occurred. More recently, molecular biologists have developed powerful tools to infer past adaptive processes, and gene expression mechanisms that describe the organization of genomes into phenotypes. Here, we argue that the evolution of endothermy could now be elucidated based on a joint, and perhaps unprecedented, effort of researchers from the fields of genomics, physiology and evolution.